Controlling unsteady locomotion; the roles of musculoskeletal properties and neural output in stability and control

        Movement need not be actively controlled to exhibit dynamic stability. For example, uncontrolled walking bipeds (McGeer, 1990) and sagittal-plane spring-mass systems (Seyfarth et al., 2002) with discontinuous stepping events can exhibit stability. In the horizontal plane, uncontrolled spring-mass models analogous to those of sagittal-plane running also exhibit stability (Schmitt and Holmes, 2000a; Schmitt and Holmes, 2000b). Parameters such as mass, moment of inertia, segment lengths, touchdown angles and segment compliance can determine the stability of an uncontrolled mechanical system (Schmitt et al., 2002; Seyfarth et al., 2002).
        Coupled with uncontrolled, or 'passive' stabilization, the action of a controller acting at step transitions can contribute to dynamic stability. Whereas passive mechanisms contribute to stabilizing bipedal locomotion in the sagittal plane, humans use lateral foot placement to stabilize the unstable lateral direction during walking (Bauby and Kuo, 2000; Mackinnon and Winter, 1993). Similar to walking, control of leg placement and stiffness at step transitions is an important part of one successful control strategy used for dynamically stable three-dimensional hopping and running robots (Raibert et al., 1984).
        An alternative to stabilizing locomotion at step transitions is to counteract perturbations within a step (Grillner, 1972; Grillner, 1975). Within-step changes in joint torques could generate forces appropriate to counteract perturbations.  Humans can modulate torque production to maintain constant-speed locomotion against an imposed force (Bonnard and Pailhous, 1991), and use changes in joint torques to counteract imposed force impulses when the impulses occur early in the step cycle (Yang et al., 1990). These dynamic changes in joint torques could serve to control about equilibrium trajectories during locomotion.
        However, as animals move faster and stride periods decrease, the time available to recover from perturbations to movement within a step period decreases (Alexander, 1982). Neural delays in sensing a perturbation, generating an appropriate motor pattern within the nervous system to arrest the perturbation, and delays involved in muscle activation and force generation could limit the effectiveness with which neural feedback systems could continuously stabilize rapid movement (Full and Koditschek, 1999; Hogan, 1990; Joyce et al., 1974; McIntyre and Bizzi, 1993; Pearson and Iles, 1973).
        Alternatively, stabilization of movement through non-neural mechanisms is also possible. Viscoelastic properties of muscles, skeletons and connective tissue, changing muscle moment arms, and the length- and velocity- dependence of force production in active muscle all have the potential to contribute to the mechanical stabilization of musculoskeletal systems (Grillner, 1975; Seyfarth et al., 2001; Wagner and Blickhan, 1999). The potentially stabilizing properties of active muscles have been termed 'preflexes', since the stabilizing behavior of musculoskeletal systems may appear similar to neural reflexes, but have the potential to occur very quickly before neural reflexes have the ability to act (Brown and Loeb, 2000). During rapid locomotion, musculoskeletal 'preflexes' could offer continuous stabilization even at very high movement frequencies, and augment reflexive stabilization generated by the nervous system.
        We seek to determine the relative roles of musculoskeletal properties and neural output in stability and control.